Grafted human neural stem cells enhance several steps of endogenous neurogenesis and improve behavioral recovery after middle cerebral artery occlusion in rats

Neurobiology of Disease

Volumn 52, Issue , 2013, Pages 191-203

  Mine, Yutaka ^a   Tatarishvili, Jemal ^a   Oki, Koichi ^a   Monni, Emanuela ^a   Kokaia, Zaal ^a   Lindvall, Olle ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Inflammation; Neurogenesis; Stem cells; Stroke; Transplantation

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL COUNT; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SUBPOPULATION; CELL SURVIVAL; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; CORPUS STRIATUM; FETUS; GLOBUS PALLIDUS; HUMAN; HUMAN CELL; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE FIBER; NERVE STIMULATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL TRANSPLANTATION; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; RAT; SUBVENTRICULAR ZONE;

ANIMALS; CELL MOVEMENT; CORPUS STRIATUM; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MOTOR SKILLS; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; RATS; RATS, NUDE; RECOVERY OF FUNCTION; WALKING;

EID: 84873568236     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.12.006     Document Type: Article

References (50)

1. Andres R.H., Horie N., Slikker W., Keren-Gill H., Zhan K., Sun G., Manley N.C., Pereira M.P., Sheikh L.A., McMillan E.L., Schaar B.T., Svendsen C.N., Bliss T.M., Steinberg G.K. Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain. Brain 2011, 134:1777-1789.
2. Arvidsson A., Collin T., Kirik D., Kokaia Z., Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 2002, 8:963-970.
3. Bacigaluppi M., Pluchino S., Jametti L.P., Kilic E., Kilic U., Salani G., Brambilla E., West M.J., Comi G., Martino G., Hermann D.M. Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 2009, 132:2239-2251.
4. Cusimano M., Biziato D., Brambilla E., Donega M., Alfaro-Cervello C., Snider S., Salani G., Pucci F., Comi G., Garcia-Verdugo J.M., De Palma M., Martino G., Pluchino S. Transplanted neural stem/precursor cells instruct phagocytes and reduce secondary tissue damage in the injured spinal cord. Brain 2012, 135:447-460.
5. Daadi M.M., Maag A.L., Steinberg G.K. Adherent self-renewable human embryonic stem cell-derived neural stem cell line: functional engraftment in experimental stroke model. PLoS One 2008, 3:e1644.
6. Daadi M.M., Li Z., Arac A., Grueter B.A., Sofilos M., Malenka R.C., Wu J.C., Steinberg G.K. Molecular and magnetic resonance imaging of human embryonic stem cell-derived neural stem cell grafts in ischemic rat brain. Mol. Ther. 2009, 17:1282-1291.
7. Darsalia V., Kallur T., Kokaia Z. Survival, migration and neuronal differentiation of human fetal striatal and cortical neural stem cells grafted in stroke-damaged rat striatum. Eur. J. Neurosci. 2007, 26:605-614.
8. Darsalia V., Allison S.J., Cusulin C., Monni E., Kuzdas D., Kallur T., Lindvall O., Kokaia Z. Cell number and timing of transplantation determine survival of human neural stem cell grafts in stroke-damaged rat brain. J. Cereb. Blood Flow Metab. 2011, 31:235-242.
9. Heldmann U., Mine Y., Kokaia Z., Ekdahl C.T., Lindvall O. Selective depletion of Mac-1-expressing microglia in rat subventricular zone does not alter neurogenic response early after stroke. Exp. Neurol. 2011, 229:391-398.
10. Horie N., Pereira M.P., Niizuma K., Sun G., Keren-Gill H., Encarnacion A., Shamloo M., Hamilton S.A., Jiang K., Huhn S., Palmer T.D., Bliss T.M., Steinberg G.K. Transplanted stem cell-secreted vascular endothelial growth factor effects poststroke recovery, inflammation, and vascular repair. Stem Cells 2011, 29:274-285.
11. Hou S.W., Wang Y.Q., Xu M., Shen D.H., Wang J.J., Huang F., Yu Z., Sun F.Y. Functional integration of newly generated neurons into striatum after cerebral ischemia in the adult rat brain. Stroke 2008, 39:2837-2844.
12. Imai Y., Kohsaka S. Intracellular signaling in M-CSF-induced microglia activation: role of Iba1. Glia 2002, 40:164-174.
13. Ito D., Tanaka K., Suzuki S., Dembo T., Fukuuchi Y. Enhanced expression of iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 2001, 32:1208-1215.
14. Jin K., Minami M., Lan J.Q., Mao X.O., Batteur S., Simon R.P., Greenberg D.A. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:4710-4715.
15. Jin K., Mao X.O., Sun Y., Xie L., Greenberg D.A. Stem cell factor stimulates neurogenesis in vitro and in vivo. J. Clin. Invest. 2002, 110:311-319.
16. Jin K., Xie L., Mao X., Greenberg M.B., Moore A., Peng B., Greenberg R.B., Greenberg D.A. Effect of human neural precursor cell transplantation on endogenous neurogenesis after focal cerebral ischemia in the rat. Brain Res. 2011, 1374:56-62.
17. Kallur T., Darsalia V., Lindvall O., Kokaia Z. Human fetal cortical and striatal neural stem cells generate region-specific neurons in vitro and differentiate extensively to neurons after intrastriatal transplantation in neonatal rats. J. Neurosci. Res. 2006, 84:1630-1644.
18. Kelly S., Bliss T.M., Shah A.K., Sun G.H., Ma M., Foo W.C., Masel J., Yenari M.A., Weissman I.L., Uchida N., Palmer T., Steinberg G.K. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11839-11844.
19. Kim K.K., Adelstein R.S., Kawamoto S. Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J. Biol. Chem. 2009, 284:31052-31061.
20. Kirik D., Rosenblad C., Bjorklund A. Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat. Exp. Neurol. 1998, 152:259-277.
21. Kirik D., Georgievska B., Rosenblad C., Bjorklund A. Delayed infusion of GDNF promotes recovery of motor function in the partial lesion model of Parkinson's disease. Eur. J. Neurosci. 2001, 13:1589-1599.
22. Kokaia Z., Zhao Q., Kokaia M., Elmer E., Metsis M., Smith M.L., Siesjo B.K., Lindvall O. Regulation of brain-derived neurotrophic factor gene expression after transient middle cerebral artery occlusion with and without brain damage. Exp. Neurol. 1995, 136:73-88.
23. Kokaia Z., Andsberg G., Martinez-Serrano A., Lindvall O. Focal cerebral ischemia in rats induces expression of P75 neurotrophin receptor in resistant striatal cholinergic neurons. Neuroscience 1998, 84:1113-1125.
24. Kokaia Z., Martino G., Schwartz M., Lindvall O. Cross-talk between neural stem cells and immune cells: the key to better brain repair?. Nat. Neurosci. 2012, 15:1078-1087.
25. Lagace D.C. Does the endogenous neurogenic response alter behavioral recovery following stroke?. Behav. Brain Res. 2012, 227:426-432.
26. Larsen J.O., Gundersen H.J., Nielsen J. Global spatial sampling with isotropic virtual planes: estimators of length density and total length in thick, arbitrarily orientated sections. J. Microsc. 1998, 191:238-248.
27. Lee S.T., Chu K., Jung K.H., Kim S.J., Kim D.H., Kang K.M., Hong N.H., Kim J.H., Ban J.J., Park H.K., Kim S.U., Park C.G., Lee S.K., Kim M., Roh J.K. Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain 2008, 131:616-629.
28. Lindvall O., Kokaia Z. Stem cell research in stroke: how far from the clinic?. Stroke 2011, 42:2369-2375.
29. Macas J., Nern C., Plate K.H., Momma S. Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain. J. Neurosci. 2006, 26:13114-13119.
30. Marti-Fabregas J., Romaguera-Ros M., Gomez-Pinedo U., Martinez-Ramirez S., Jimenez-Xarrie E., Marin R., Marti-Vilalta J.L., Garcia-Verdugo J.M. Proliferation in the human ipsilateral subventricular zone after ischemic stroke. Neurology 2010, 74:357-365.
31. Minger S.L., Ekonomou A., Carta E.M., Chinoy A., Perry R.H., Ballard C.G. Endogenous neurogenesis in the human brain following cerebral infarction. Regen. Med. 2007, 2:69-74.
32. Molina C.A. Reperfusion therapies for acute ischemic stroke: current pharmacological and mechanical approaches. Stroke 2011, 42:S16-S19.
33. Oki K., Tatarishvili J., Woods J., Koch P., Wattananit S., Mine Y., Monni E., Prietro D.T., Ahlenius H., Ladewig J., Brustle O., Lindvall O., Kokaia Z. Human induced pluripotent stem cells form functional neurons and improve recovery after grafting in stroke-damaged brain. Stem Cells 2012, 30:1120-1133.
34. Parent J.M., Vexler Z.S., Gong C., Derugin N., Ferriero D.M. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol. 2002, 52:802-813.
35. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1997, Academic Press, San Diego, CA.
36. Schallert T., Fleming S.M., Leasure J.L., Tillerson J.L., Bland S.T. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000, 39:777-787.
37. Sun X., Zhang Q.W., Xu M., Guo J.J., Shen S.W., Wang Y.Q., Sun F.Y. New striatal neurons form projections to substantia nigra in adult rat brain after stroke. Neurobiol. Dis. 2012, 45:601-609.
38. Thored P., Arvidsson A., Cacci E., Ahlenius H., Kallur T., Darsalia V., Ekdahl C.T., Kokaia Z., Lindvall O. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 2006, 24:739-747.
39. Thored P., Wood J., Arvidsson A., Cammenga J., Kokaia Z., Lindvall O. Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 2007, 38:3032-3039.
40. Thored P., Heldmann U., Gomes-Leal W., Gisler R., Darsalia V., Taneera J., Nygren J.M., Jacobsen S.E., Ekdahl C.T., Kokaia Z., Lindvall O. Long-term accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 2009, 57:835-849.
41. Wang Z., Andrade N., Torp M., Wattananit S., Arvidsson A., Kokaia Z., Jorgensen J.R., Lindvall O. Meteorin is a chemokinetic factor in neuroblast migration and promotes stroke-induced striatal neurogenesis. J. Cereb. Blood Flow Metab. 2012, 32:387-398.
42. Wang X., Mao X., Xie L., Sun F., Greenberg D.A., Jin K. Conditional depletion of neurogenesis inhibits long-term recovery after experimental stroke in mice. PLoS One 2012, 7:e38932.
43. West M.J. Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci. 1999, 22:51-61.
44. Westin J.E., Lindgren H.S., Gardi J., Nyengaard J.R., Brundin P., Mohapel P., Cenci M.A. Endothelial proliferation and increased blood-brain barrier permeability in the basal ganglia in a rat model of 3,4-dihydroxyphenyl-l-alanine-induced dyskinesia. J. Neurosci. 2006, 26:9448-9461.
45. Wictorin K., Brundin P., Gustavii B., Lindvall O., Björklund A. Reformation of long axon pathways in adult rat central nervous system by human forebrain neuroblasts. Nature 1990, 347:556-558.
46. Yamashita T., Ninomiya M., Hernandez Acosta P., Garcia-Verdugo J.M., Sunabori T., Sakaguchi M., Adachi K., Kojima T., Hirota Y., Kawase T., Araki N., Abe K., Okano H., Sawamoto K. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J. Neurosci. 2006, 26:6627-6636.
47. Yasuhara T., Matsukawa N., Hara K., Yu G., Xu L., Maki M., Kim S.U., Borlongan C.V. Transplantation of human neural stem cells exerts neuroprotection in a rat model of Parkinson's disease. J. Neurosci. 2006, 26:12497-12511.
48. Zhang R., Zhang Z., Wang L., Wang Y., Gousev A., Zhang L., Ho K.L., Morshead C., Chopp M. Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J. Cereb. Blood Flow Metab. 2004, 24:441-448.
49. Zhang P., Li J., Liu Y., Chen X., Lu H., Kang Q., Li W., Gao M. Human embryonic neural stem cell transplantation increases subventricular zone cell proliferation and promotes peri-infarct angiogenesis after focal cerebral ischemia. Neuropathology 2011, 31:384-391.
50. Zhao Q., Smith M.-L., Siesjö B.K. The w-conopeptide SNX-111, an N-type calcium channel blocker, dramatically ameliorates brain damage due to transient focal ischaemia. Acta Physiol. Scand. 1994, 150:459-461.